Regional distribution patterns predict bird occurrence in Mediterranean cropland afforestations Luis M. Carrascal, Ismael Galván, Juan S. Sánchez-Oliver & José M. Rey Benayas
Ecological Research ISSN 0912-3814 Volume 29 Number 2 Ecol Res (2014) 29:203-211 DOI 10.1007/s11284-013-1114-1
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Author's personal copy Ecol Res (2014) 29: 203–211 DOI 10.1007/s11284-013-1114-1
O R I GI N A L A R T IC L E
Luis M. Carrascal • Ismael Galva´n • Juan S. Sa´nchez-Oliver • Jose´ M. Rey Benayas
Regional distribution patterns predict bird occurrence in Mediterranean cropland afforestations
Received: 22 April 2013 / Accepted: 28 November 2013 / Published online: 20 December 2013 The Ecological Society of Japan 2013
Abstract Part of the abandoned cropland in Mediterranean landscapes is being subjected to afforestation dominated by pines. Here we simultaneously evaluate the effect of three categories of factors as predictors of the interspecific variation in bird habitat occupancy of fragmented afforestations, namely regional distribution, habitat preferences, and life-history traits of species. We use the ‘‘natural experiment’’ that highly fragmented pine plantations of central Spain represent due to the prevailing pattern of land ownership of small properties. Many species with marked habitat preferences for woodland habitats were very scarce or were never recorded in this novel habitat within a matrix of deforested agricultural landscape. Interspecific variability in occurrence was mainly explained by regional distribution patterns: occurrence was significantly and positively associated with the proportion of occupied 10 · 10 UTM km squares around the study area, habitat breadth, and population trend of species in the period 1998–2011. It was also positively associated with regional occupancy of mature and large pine plantations. Other predictor variables related to habitat preferences (for woodland, agricultural and urban habitats) or life-history traits (migratory
Electronic supplementary material The online version of this article (doi:10.1007/s11284-013-1114-1) contains supplementary material, which is available to authorized users. L. M. Carrascal (&) Departamento de Biogeografı´ a y Cambio Global, Museo Nacional de Ciencias Naturales (MNCN-CSIC), Jose´ Gutie´rrez Abascal 2, 28006 Madrid, Spain E-mail:
[email protected] I. Galva´n Centro de Biologia Ambiental, Universidade de Lisboa, Edifı´ cio C2, Campo Grande, 1749-016 Lisboa, Portugal J. S. Sa´nchez-Oliver Æ J. M. Rey Benayas Departamento de Ciencias de la Vida, UD Ecologı´ a, Universidad de Alcala´, Edificio de Ciencias, Ctra. de Barcelona km 33,600, 28871 Alcala´ de Henares, Spain
strategy, body mass, and clutch size) were unrelated to the occurrence of species. Thus, small man-made pinewood islands funded by the Common Agrarian Policy within a landscape dominated by Mediterranean agricultural habitats only capture widespread and habitat generalist avian species with increasing population trends, not contributing to enhance truly woodland species. Keywords Bird occurrence Æ Cropland abandonment Æ Habitat preferences Æ Pine plantations Æ Regional distribution
Introduction Afforestation represents a strategy to produce forest land on abandoned cropland that avoids the long time that secondary succession usually takes, particularly in the drylands of the world (Rey Benayas and Bullock 2012). In the European Union, the Common Agrarian Policy (CAP) has favored the transformation of farmland into tree plantations since 1992 by means of a scheme of aid for forestry measures in agriculture (EEC Council Regulation No. 2080/92), which has resulted in the afforestation of >8 million ha to date (DirectorateGeneral for Agriculture and Rural Development 2012). These afforested fields, which in southern Europe are mostly based on coniferous species such as Pinus halepensis and P. pinaster, usually form an archipelago of habitat patches in the dominant agricultural matrix (Izhaki 1999; van Meijl et al. 2006). These afforestations impact biodiversity because pine plantations have higher tree cover and less structural heterogeneity than natural Mediterranean woodlands (Sirami et al. 2007; Rey Benayas et al. 2010). Birds represent the group of vertebrates upon which these impacts have been most intensively studied, and are good indicators of the success of colonization of these afforestations because they are highly mobile animals that easily reach these novel ecosystems. It is widely
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known that the age, area, and habitat structure of woodland islands are tightly related to species richness and bird community composition of pine plantations (e.g., Dı´ az et al. 1998; Shochat et al. 2001). Nevertheless, little is known about the filtering processes determining the identity of species occupying pine plantations within the regional pool of species in Mediterranean landscapes dominated by agricultural habitats. Three major types of effects may determine bird species identity in Mediterranean cropland afforestations, namely regional distribution patterns, habitat preferences of species and autoecological traits related to life history. Species with high density are more likely to be included in habitat fragments than scarce ones as a consequence of their abundance (Connor and McCoy 1979; Andre´n 1999), and thus bird communities inhabiting afforested fields would represent random subsets of the regional species pool independently of any ecological process. In fact, density seems to be a good predictor of the probability of species’ presence in forest fragments (e.g., Bolger et al. 1991; Tellerı´ a and Santos 1997, 1999). Additionally, species that tolerate a relatively wide range of ecological conditions are in turn more widespread and are able to occupy a large variety of habitats (Swihart et al. 2003; Bohning-Gaese et al. 2006; Hurlbert and White 2007; Carrascal et al. 2008). Therefore, pine plantations within a matrix of arable land would not selectively filter species according to the habitat characteristics of the plantations, but they would be occupied by those eurytopic species that are highly spread and abundant in the region. However, pine plantations could impose a selective filter to the colonization by the species of the regional pool according to their strict habitat selection and spatial niches (e.g., preferences for pine foliage or trunks for foraging or nesting). The habitat requirements of bird species that are characteristic of the dominant agricultural environments, or of Mediterranean habitats with marked preferences for broadleaf sclerophyllous foliage or for a well-developed understory (e.g., Tellerı´ a et al. 1999), contrast with structural characteristics provided by coniferous plantations with a generally poor shrub layer. Therefore, the habitat-matching hypothesis predicts that habitat structure of afforestations would constrain its colonization by the regional pool of species, favoring only those birds that exhibit a marked preference for coniferous trees and a high cover of the tree canopy (Santos et al. 2006; Sirami et al. 2008a, b; Rey Benayas et al. 2010). Moreover, birds may have a higher colonization success of pine plantations, in a landscape dominated by arable lands, if they are able to survive in human-altered novel habitats such as urban environments. Several studies have shown that urban-exploiter birds have larger brains than urban-avoider species (Maklakov et al. 2011), probably because large-brained animals are behaviorally innovative species that have higher success and experience lower mortality when exposed to a novel environment (Sol et al. 2005a, 2007, 2008).
Some autoecological traits of bird species, such as sedentariness, body mass, and clutch size may also predict the colonization success of pine plantations within the matrix of arable lands. Smaller birds usually attain high local and regional densities according to the inverse allometric relationship ‘body mass–population density’ (Carrascal and Tellerı´ a 1991; Gaston and Blackburn 2000), a pattern more pronounced in assemblages exploiting foliage or in habitats with a high foliage volume, in which smaller bird species predominate because of ecomorphological constraints (low body mass for hovering and hanging; e.g., Tellerı´ a and Carrascal 1994). Moreover, small body size is a predictor of establishment success across species (Cassey 2001) and is inversely related to extinction susceptibility in birds (Gaston and Blackburn 1995; Owens and Bennett 2000). Species that are sedentary and have large clutch sizes are more likely to occupy pine plantations, as these species are more likely to visit and explore the ecological opportunities provided by afforestation on a year-round basis and may attain high rates of population growth (Galva´n and Rey Benayas 2011), whereas migratory species tend to rely more on innovative feeding behaviors in winter when food is harder to find (Sol et al. 2005b). In short, the factors that affect the success of pine plantations as a restoration strategy in Mediterranean croplands, as reflected by the capacity to hold bird species, can be divided into passive processes and active filters related to habitat requirements and preferences and autoecological traits of the bird species. Here we evaluate interspecific differences in bird species occurrence in the novel insular habitat provided by small and young pine plantations of central Spain, established over a predominantly treeless landscape dominated by herbaceous or woody cultures, where large mature forests of Holm Oak Quercus rotundifolia that may serve as sources of woodland bird species are very scarce. This habitat consists of an archipelago of young and small afforestations that punctuates the agricultural landscape, because it has been favored by the EU CAP in the early 1990s, and the size of the cropped fields is usually small (20 cm dbh (# in 0.2 ha) Cover of shrubs (%) Average shrub height (m) Cover of the herbaceous layer (%)
4.6 50.6 4.7 79.5 2.7 2.8 0.9 46.1
3.7 24.1 1.0 42.2 5.7 7.2 1.0 39.2
1.3 15.3 3.5 16.0 0.0 0.0 0.0 0.0
21.9 100.0 7.2 168.0 26.0 31.7 2.9 100.0
Landscape cover around plantations (%) Streams rivers and lagoons Roads and rural tracks Woodlands Holm Oak Woodland Pine plantations Fruit groves Waste lands Olive groves Pastures with scattered trees Scrubland Pastures Dry herbaceous cropland Vineyards Vineyards with olive trees Dried fruit orchards Urban areas and scattered buildings
0.8 7.1 3.9 0.8 3.1 1.1 7.1 18.1 0.3 10.2 1.3 19.7 22.3 5.4 0.8 1.8
1.3 5.2 4.1 1.5 2.6 1.3 4.2 21.8 0.4 7.3 1.6 8.8 14.2 9.6 2.3 1.9
0.0 0.2 0.4 0.0 0.4 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
4.3 22.1 18.9 7.4 11.5 5.3 13.3 68.9 2.0 28.4 7.7 37.7 45.4 33.6 9.5 6.7
Bird censuses First, all pine plantations in the study area were located using both ortophotos (see source above) and Google Earth, and were later verified in the field. We found 100 pine plantations that took place in 1992 or later. Next, we selected the plantations to be surveyed for birds, considering those with pines taller than 3.5 m and area larger than 1 ha (31 plantations; Fig. 1), which were 12–18 years old. Details on habitat structure of the 31 study pine plantations are shown in Table 1. To asses bird occurrence in the novel habitat defined by the archipelago of pine plantations, bird censuses were carried out in spring (April and May) 2011. We did not intend to exhaustively census all the area covered by each single studied plantation because our goal was not to characterize species richness, but to establish a protocol to quantify species occurrence in the investigated novel habitat (for details on spatial variation of bird species richness with area of pine plantations in the study region, see Dı´ az et al. 1996 and Santos et al. 2006). Thus, only one census plot was established in each one of the 31 pine plantations in order to avoid pseudoreplication when quantifying relative abundance of bird species in this novel habitat. We assessed the occurrence of bird species in these census plots using point-count stations (Bibby et al. 2000) lasting 10 min. All auditory and visual contacts were recorded, but only those within a 50-m radius (0.78 ha) were used in subsequent analyses, in order to increase the detection probability of studied species. Every census plot was surveyed twice on different days, once in the morning between sunrise and 3 h later and once in the evening 2 h before sunset. All
censuses were conducted by the same well-trained field ornithologist (JSSO) on windless (wind speed 0.24; Table 2).
Discussion This study clearly shows that woodland restoration based on small, highly fragmented pine plantations in a Mediterranean landscape matrix dominated by agricultural habitats does not contribute to enhancing avian diversity by capturing woodland birds, especially if the natural forests of the region do not belong to the coniferous vegetation domain. Under these circumstances, the chance of encountering a particular species in pine plantations is the consequence of the pattern of regional distribution, instead of ecological processes mediated by preferences for a particular subset of habitats or life-history traits, where the most widespread species with broader habitat preferences (eurytopic taxa) and increasing population trends are favored. Table 2 Generalized linear regression model (with negative binomial errors and the log-link function) relating the habitat occupancy of 80 bird species in young and small pine plantations of agricultural areas of central Spain and ten predictor variables describing regional distribution, habitat breadth, population trends (1998–2011), regional habitat preferences (four variables), migratory strategy, body mass, and clutch size Coefficientd Regional distributionb Habitat breadth Population trend (1998–2011) Occupation index of mature plantationsb Relative abundance in woodlands Relative abundance in agricultural habitats Relative abundance in urban environments Migratory strategyc Body mass (in ln) Clutch size
SE
pa
1.03 0.94 0.39 0.25
0.53 0.36 0.12 0.10
0.050 0.009 25 ha; Galva´n and Rey Benayas 2011), so processes controlling their colonization by birds cannot be straightforward compared. Future studies should investigate if bird occurrence and density are actually dependent on different factors in Mediterranean cropland afforestations. In conclusion, pine plantations favored by the European CAP resulting in an archipelago of man-made woodland islands within a Mediterranean agricultural landscape, only capture widespread and habitat generalist avian species with increasing population trends, not contributing to favoring truly woodland species. This result casts doubts on the value of this restoration practice for the conservation and management of avian diversity in the Mediterranean region if it is developed in very small woodland areas considering the pattern of land tenure of small properties. Acknowledgments Projects from the Spanish Ministry of Science and Education (CGL2010-18312) and the Government of Madrid (S2009AMB-1783, REMEDINAL-2) are currently providing financial support for this body of research. The Fundacio´n Internacional para la Restauracio´n de Ecosistemas has supported JSSO. Claire Jasinski kindly improved the English of the manuscript. Comments from three anonymous reviewers improved a previous version of this manuscript.
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